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1. Functional analysis of LHCSR1, a protein catalyzing NPQ in mosses, by heterologous expression in Arabidopsis thaliana

Author

Alberta Pinnola, Ioannis Dikaios, Alessandro Alboresi, Christo Schiphorst, Roberto Bassi, and Luca Dall'Osto

Subjects
0106 biological sciences, 0301 basic medicine, NPQ, Light, LHCSR, Zeaxanthin epoxidase, Arabidopsis, Light-Harvesting Protein Complexes, Plant Science, Xanthophylls, Physcomitrella patens, Thylakoids, 01 natural sciences, Biochemistry, 03 medical and health sciences, Gene Expression Regulation, Plant, Zeaxanthins, Photosynthesis, A. thaliana, Heterologous expression, P. patens, Photoprotection, Chlorophyll fluorescence, Plant Proteins, chemistry.chemical_classification, biology, Chemistry, food and beverages, Cell Biology, General Medicine, Photochemical Processes, Plants, Genetically Modified, biology.organism_classification, Bryopsida, Recombinant Proteins, Chloroplast, 030104 developmental biology, Thylakoid, Xanthophyll, Mutation, Biophysics, biology.protein, Original Article, Oxidoreductases, 010606 plant biology & botany
Abstract

Non-photochemical quenching, NPQ, of chlorophyll fluorescence regulates the heat dissipation of chlorophyll excited states and determines the efficiency of the oxygenic photosynthetic systems. NPQ is regulated by a pH-sensing protein, responding to the chloroplast lumen acidification induced by excess light, coupled to an actuator, a chlorophyll/xanthophyll subunit where quenching reactions are catalyzed. In plants, the sensor is PSBS, while the two pigment-binding proteins Lhcb4 (also known as CP29) and LHCII are the actuators. In algae and mosses, stress-related light-harvesting proteins (LHCSR) comprise both functions of sensor and actuator within a single subunit. Here, we report on expressing the lhcsr1 gene from the moss Physcomitrella patens into several Arabidopsis thaliana npq4 mutants lacking the pH sensing PSBS protein essential for NPQ activity. The heterologous protein LHCSR1 accumulates in thylakoids of A. thaliana and NPQ activity can be partially restored. Complementation of double mutants lacking, besides PSBS, specific xanthophylls, allowed analyzing chromophore requirement for LHCSR-dependent quenching activity. We show that the partial recovery of NPQ is mostly due to the lower levels of Zeaxanthin in A. thaliana in comparison to P. patens. Complemented npq2npq4 mutants, lacking besides PSBS, Zeaxanthin Epoxidase, showed an NPQ recovery of up to 70% in comparison to A. thaliana wild type. Furthermore, we show that Lutein is not essential for the folding nor for the quenching activity of LHCSR1. In short, we have developed a system to study the function of LHCSR proteins using heterologous expression in a variety of A. thaliana mutants. Electronic supplementary material The online version of this article (10.1007/s11120-019-00656-3) contains supplementary material, which is available to authorized users.

Published
2019

2. A systems-wide understanding of photosynthetic acclimation in algae and higher plants

Author

Roberto Bassi, Ioannis Dikaios, Brieuc Urbain, Michel Goldschmidt-Clermont, Oliver Ebenhöh, Anna Matuszyńska, Stephanie Spelberg, Julie Maguire, Kailash Adhikari, Adeline Le Monnier, Dipali Singh, Stefano Magni, Giulio Rocco Stella, Lucilla Taddei, Federica Cariti, Claudia Zabke, Fiona Wanjiku Moejes, Antonella Succurro, Kathrin Müller, Giovanni Finazzi, Mark G. Poolman, Valeria Villanova, Serena Flori, Guillaume Cogne, Angela Falciatore, Cluster of Excellence on Plant Sciences (CEPLAS), Institute of Quantitative and Theoretical Biology, Heinrich Heine Universität Düsseldorf = Heinrich Heine University [Düsseldorf], Bantry Marine Research Station, Department of Biological and Medical Sciences, Oxford Brookes University, Department of Biotechnology, University of Tehran-University College of Science, Department of Botany and Plant Biology, University of Geneva, Laboratoire de génie des procédés - environnement - agroalimentaire (GEPEA), Institut Universitaire de Technologie - Nantes (IUT Nantes), Université de Nantes (UN)-Université de Nantes (UN)-Université de Nantes - UFR des Sciences et des Techniques (UN UFR ST), Université de Nantes (UN)-Université de Nantes (UN)-Institut Universitaire de Technologie Saint-Nazaire (IUT Saint-Nazaire), Université de Nantes (UN)-Ecole Polytechnique de l'Université de Nantes (EPUN), Université de Nantes (UN)-Ecole Nationale Vétérinaire, Agroalimentaire et de l'alimentation Nantes-Atlantique (ONIRIS)-Centre National de la Recherche Scientifique (CNRS)-Université Bretagne Loire (UBL)-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Institut Universitaire de Technologie - La Roche-sur-Yon (IUT La Roche-sur-Yon), Université de Nantes (UN), Centre National de la Recherche Scientifique (CNRS), Ecole Nationale Vétérinaire Agroalimentaire et de l'Alimentation Nantes Atlantique (ONIRIS), PRES Université Nantes Angers Le Mans (UNAM), Biologie Computationnelle et Quantitative = Laboratory of Computational and Quantitative Biology (LCQB), Institut de Biologie Paris Seine (IBPS), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Université Pierre et Marie Curie - Paris 6 (UPMC), Sorbonne Université (SU), UMR 1417 PCV Laboratoire de Physiologie Cellulaire Végétale., Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Institut National de la Recherche Agronomique (INRA), Université Grenoble Alpes [2016-2019] (UGA [2016-2019]), Fermentalg SA, IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT), University of Aberdeen, Marie Curie Initial Training Network project, AccliPhot [PITN-GA-2012-316427], Université de Nantes - UFR des Sciences et des Techniques (UN UFR ST), Université de Nantes (UN)-Université de Nantes (UN)-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Centre National de la Recherche Scientifique (CNRS)-Ecole Polytechnique de l'Université de Nantes (EPUN), Université de Nantes (UN)-Université de Nantes (UN)-Institut Universitaire de Technologie - Nantes (IUT Nantes), Université de Nantes (UN)-Institut Universitaire de Technologie Saint-Nazaire (IUT Saint-Nazaire), Université de Nantes (UN)-Institut Universitaire de Technologie - La Roche-sur-Yon (IUT La Roche-sur-Yon), Université de Nantes (UN)-Ecole Nationale Vétérinaire, Agroalimentaire et de l'alimentation Nantes-Atlantique (ONIRIS)-Université Bretagne Loire (UBL), Heinrich-Heine-Universität Düsseldorf [Düsseldorf], Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Université Pierre et Marie Curie (Paris 6), Sorbonne Universités, Université Grenoble Alpes (UGA), Ecole Nationale Supérieure des Mines de Nantes (Mines Nantes), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut de Biologie Paris Seine (IBPS), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Université de Nantes (UN)-École nationale vétérinaire, agroalimentaire et de l'alimentation Nantes-Atlantique (ONIRIS)-Centre National de la Recherche Scientifique (CNRS)-Université Bretagne Loire (UBL)-IMT Atlantique (IMT Atlantique), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), IMT Atlantique (IMT Atlantique), Moejes F.W., Matuszynska A., Adhikari K., Bassi R., Cariti F., Cogne G., Dikaios I., Falciatore A., Finazzi G., Flori S., Goldschmidt-Clermont M., Magni S., Maguire J., Le Monnier A., Muller K., Poolman M., Singh D., Spelberg S., Stella G.R., Succurro A., Taddei L., Urbain B., Villanova V., Zabke C., and Ebenhoh O.

Subjects
0301 basic medicine, [SDV.BIO]Life Sciences [q-bio]/Biotechnology, Physiology, Acclimatization, Context (language use), PhD training, interdisciplinary training, Plant Science, Biochemistry, biophysics & molecular biology [F05] [Life sciences], Biology, acclimation, Photosynthesis, Models, Biological, modelling, 03 medical and health sciences, Algae, Chlorophyta, application industrielle, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, mathematical modelling, Biochimie, biophysique & biologie moléculaire [F05] [Sciences du vivant], biodiversity, modélisation, micro-algue, Phototroph, photosynthetic system, Ecology, Non-photochemical quenching, Systems Biology, acclimatation photosynthétique, photosynthetic optimisation, Plankton, Plants, analyse rétrospective, biology.organism_classification, industrial application, European Training Network, 030104 developmental biology, Acclimation, microalgal cultivation, non-photochemical quenching, Photosynthetic acclimation, adaptation à la lumière, appareil photosynthétique, Biochemical engineering
Abstract

The ability of phototrophs to colonise different environments relies on robust protection against oxidative stress, a critical requirement for the successful evolutionary transition from water to land. Photosynthetic organisms have developed numerous strategies to adapt their photosynthetic apparatus to changing light conditions in order to optimise their photosynthetic yield, which is crucial for life on Earth to exist. Photosynthetic acclimation is an excellent example of the complexity of biological systems, where highly diverse processes, ranging from electron excitation over protein protonation to enzymatic processes coupling ion gradients with biosynthetic activity, interact on drastically different timescales from picoseconds to hours. Efficient functioning of the photosynthetic apparatus and its protection is paramount for efficient downstream processes, including metabolism and growth. Modern experimental techniques can be successfully integrated with theoretical and mathematical models to promote our understanding of underlying mechanisms and principles. This review aims to provide a retrospective analysis of multidisciplinary photosynthetic acclimation research carried out by members of the Marie Curie Initial Training Project, AccliPhot, placing the results in a wider context. The review also highlights the applicability of photosynthetic organisms for industry, particularly with regards to the cultivation of microalgae. It intends to demonstrate how theoretical concepts can successfully complement experimental studies broadening our knowledge of common principles in acclimation processes in photosynthetic organisms, as well as in the field of applied microalgal biotechnology.

Published
2017
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